A Review of the Literature of the Neofabraea Species Complex, Causative Agents of Gloeosporium Rot in Stored Apple

A review of the literature of the Neofabraea species complex, causative agents of Gloeosporium rot in stored apple Robert Saville, East Malling Research, East Malling, Kent, ME19 6BJ Apples are stored for up to 12 months following harvest and are subject to attack from numerous post- harvest pathogens. Neofabraea species are considered an important post-harvest disease worldwide and losses of up to 35% have been reported for this disease (Sutton et al., 2014). An apple rot survey of UK pac houses undertaken from 2008 - 2013 as part of Horticultural Development Company (HDC) projects TF193 and CP90, identified an increasing incidence in the occurrence of fruit rot caused by Neofabraea species in stored apples over the duration of the survey. On this basis the HDC commissioned this literature review of the fungus responsible and the current control options available, to inform future research into this disease. Figure 1. Left: Apple rot; Top right: Neofabraea alba colony morphology; Middle right: Neofabraea alba spores; Bottom right: N.perennans/N.malicorticis symptoms. Contents Section Page Importance of the fungus 1 The fungus 3 Neofabraea species identification ; a UK case study 8 Epidemiology 12 Host interactions 12 Control 13 Future research needs 15 Main points for growers 15 Acknowledgements 16 References 16 Importance of the fungus pollination Losses in store Neofabraea species can induce wood lesions on trees in the orchard but it is the post-harvest rot that develops in the store where the majority of losses due to this fungus are experienced. The fungus characteristically gains entry to developing fruit in the orchard through the lenticels and can remain latent for some time after harvest. In the UK, fruit rot caused by Neofabraea species in store has changed in significance over the years, the level and frequency depending on seasonal weather conditions and cultural factors in the orchard and/or changes in store practice. Apple rot surveys carried out in the UK have revealed a rise and fall in the prevalence of this disease in store over the last century. In the 1920’s, Neofabraea (then referred to as Gloeosporium) was recorded in a comprehensive survey of rots developing in store on Bramley’s seedling among other cultivars (Kidd and Beaumont, 1924). Although quantitative data was not reported on the incidence of the rot, the authors state that Neofabraea (alba) was ‘one of the less frequent fungi’ recorded in the survey. Conversely, a survey in the 1930’s, sampling numerous apple cultivars from the main fruit growing areas of England (Wilkinson, 1954), recorded Neofabraea as the predominant rot developing in store in 1937/8 and 1938/9 (Figure 1). In the 1960’s, just prior to the introduction of post-harvest fungicide treatments and the large scale adoption of controlled atmosphere storage across the industry, losses of up to 50% were recorded in some consignments of Cox, mainly due to rotting caused by Neofabraea species (Preece, 1967). Figure 2. An excerpt from Wilkinson (1954) which showed that Neofabraea (Gloeosporium species as it was then known) was the predominant rot developing on cold stored apples in the 1930’s. Apple rot surveys undertaken in the 1980’s show that fruit rot caused by Neofabraea species was reduced to trace levels in most of the years surveyed and this rot was only a problem when fruit nutrition was sub- optimal (Berrie, 1989). Berrie (1993) attributed the decline in the significance of Neofabraea rot to ‘the introduction of post-harvest fungicide treatments, combined with improved storage of fruit and a better understanding of the importance of fruit mineral composition in preserving fruit quality’. With the phasing out of the practice of post-harvest fungicide treatment, Berrie (1993) demonstrated alternative control strategies to mitigate losses due to storage rots in an era without post-harvest fungicide treatments. The efficacy of pre-harvest fungicide treatments were tested against post-harvest fungicide treatments and initial data was presented on the rot risk assessment concept which determines treatment according to need (Berrie, 1993). 1 Following a decline in the incidence of fruit rot caused by Neofabraea species in the 1990s to negligible levels in the UK, a recent increase has been observed. During the most recent survey, spanning 2008- 2013 growing seasons, undertaken as part of HDC project TF193 (Sustainable control of storage rots of apple, 2008-2010) and the HDC fellowship project CP90 (Succession planning to sustain the UKs expertise in field and laboratory plant pathology research and development, 2011-present), fruit rot caused by Neofabraea species has been increasing in incidence in all apple cultivars surveyed. In 2010 and 2011 the percentage of apple samples surveyed which contained fruit rot caused by Neofabraea, was on average between 80 and 100% on susceptible cultivars (Figure 2b). Against this trend, the incidence in the 2013 rot survey dropped significantly (average incidence for susceptible cultivars = 56%) and further still (16%) in the 2014 survey. A historic resume of the rot surveys discussed in this section is presented in Figure 2a. Figure 2. The rise and fall of Neofabraea rot incidence in the UK. (a) Data compiled from four rot surveys spanning the last 75 years. The data set is for Cox, as this is the common cultivar recorded across all surveys (1Wilkinson, 1984, 2Preece, 1967, 3Berrie, 1989, 4Saville, 2013, † Average total losses due to rots during survey period). The categorisation of taxa in the legend are described as recorded in the literature so some inconsistencies between data sets are present i.e. Sclerotinia frutigena is the same as Monillinia fructigina and rots have been grouped in certain surveys (e.g. ‘other rots’). As far as possible common colour coding has been used to represent these inconsistencies. Figure 2 (b) Neofabraea incidence of four susceptible cultivars in rot surveys spanning 2008-2013 growing seasons. The graph shows the percentage of apple samples with Neofabraea (Gloeosporium) - Data from Berrie, 2010 and Saville, 2013. 2 The recent rise and fall of fruit rots caused by Neofabraea species could have many explanations including; i. Trends in fungicide use – post-harvest treatments were replaced by pre-harvest treatments (Bellis/Switch/Geoxe) which have been increasingly used in recent years due to conditions favourable to storage rots. ii. Changes in orchard practice leading to an increase/decrease in inoculum availability. iii. Variability in climatic conditions across growing seasons affecting inoculum availability, infection and nutrient uptake. iv. Late harvests leading to reduced time in store for symptom expression from harvest to assessment (the survey period is fixed, spanning from January – March). v. Changes in management practice for other targets (‘primary’ disease) influencing the significance of Neofabraea species (‘secondary’ disease). All of the above factors will be further explored in the subsequent sections of this review. Fruit rot caused by Neofabraea species is the principal cause of decay of stored apple in Europe as reported in France (Bompeix et al., 2000), Norway (Landfald, 1983) and Germany (Maxin et al., 2005). The disease is also significant in North America. For example in British Columbia, a survey of packhouses revealed that bull’s-eye rot accounted for 40% of diseased Golden Delicious apples and 9% of diseased McIntosh apples (Sholberg and Haag, 1996). The wood lesions caused by this disease can also be a serious problem in climates which favour the disease. For example in the Fraser valley, British Columbia, Neofabraea canker incidence on a per tree basis was reported to be between 50 and 80% (Rahe, 1997). Reports of losses of pear in USA between 5 and 50% (Lennox et al., 2004) highlight the potentially significant economic losses that can be caused by Neofabraea species. The fungus pollination Nomenclature Historically the Neofabraea species as we know them today have been ascribed to various taxonomic classifications. Verkley (1999) provides a comprehensive overview of Pezicula, the genus to which Neofabraea species used to belong and provides evidence based on molecular taxonomy, that Neofabraea is a separate evolutionary lineage. Neofabraea is a genus containing seven species; Neofabraea malicorticis, Neofabraea corticola, Neofabraea perennans, Neofabraea alba, Neofabraea krawtzewii, Neofabraea populi and Neofabraea eucalypti. An eighth species, Cryptosporiopsis kienholzii, previously referred to in the literature as Neofabraea sp. nov. (De Jong et al., 2001) until the naming of the anamorphic state (Spotts, 2009), is a recent addition to this genus. All are pathogens of woody hosts and Neofabraea malicorticis, Neofabraea perennans, Neofabraea alba and Cryptosporiopsis kienholzii are pathogenic on Malus and Pyrus species. The numerous synonyms and previous taxonomy classifications of the telomorphs and anamorphs of these fungi are described in Table 1. Colletotrichum acutatum is also included in this table because this species has historically been grouped within Gloeosporium (Gloeosporium fuctigenum). Symptoms caused on the host The wood lesions caused by Neofabraea spp. are variously referred to dependent on the causative casual organism. Anthracnose canker, caused by Neofabraea malicorticis and to a lesser extent by N. alba (which require wounding to infect), first appears as small circular red-purple spots. As they enlarge they become elliptical, sunken and orange-brown

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